Antimicrobial resistance pattern of Salmonella spp. isolated from poultry farms in Abakaliki, Nigeria

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EMMANUEL NNABUIKE UGBO
MUSTOFA HELMI EFFENDI
ADIANA MUTAMSARI WITANINGRUM
WIWIEK TYASNINGSIH
BERNARD NNABUIFE AGUMAH
AGATHA IFUNANYA UGBO
CHARITY CHINYERE NNABUGWU
DIVINEGIFT OLUCHI OKATA-NWALI

Abstract

Abstract. Ugbo EN, Effendi MH, Witaningrum AM, Tyasningsih W, Agumah BN, Ugbo AI, Nnabugwu CC, Okata-Nwali DO. 2023. Antimicrobial resistance pattern of Salmonella spp. isolated from poultry farms in Abakaliki, Nigeria. Biodiversitas 24: 5207-5214. Salmonella is a zoonotic foodborne pathogen that can cause serious illness in humans and animals worldwide. Antimicrobial resistance caused by microorganisms has greatly challenged veterinary and human medicine regarding disease treatments. The objective of this study was to evaluate the antimicrobial resistance pattern of Salmonella spp. isolated from poultry farms in Abakaliki, Nigeria. One hundred eighty samples (90 broiler feces; 90 broiler cloacal swabs) were collected from three (3) poultry farms in the Abakaliki metropolis. Samples were analyzed and identified for the presence of Salmonella isolates using standard microbiological and biochemical analysis. The antimicrobial sensitivity test of Salmonella isolates against the selected antibiotics was done using the Kirby-Bauer disk diffusion method on Mueller Hinton agar. The results showed 61 samples (33.9 %) were positive for Salmonella. Feces and cloacal swab samples positive for Salmonella were 46.7% and 21.1%, respectively. Multidrug resistance Salmonella (MDR) strains had an overall prevalence of samples (16.2%), i.e., 7 samples of broiler feces had 7 (16.7%) and 3 samples of cloacal swab (15.8%). Thus, all the MDR Salmonella isolates were 100% resistant to tetracycline and ampicillin. The multiple antibiotic-resistant indexes of the MDR were 0.51. This study indicated that broilers chicken and their products were potential sources of human salmonellosis and sources for transmitting MDR Salmonella in Abakaliki, Nigeria. Poultry farmers should use antibiotics in appropriate dosages in their poultry farms.

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References
Abd El-Aziz NK, Tartor YH, Gharieb RMA, Erfan AM, Khalifa E, Said MA, Ammar AM, Samir M. 2021. Extensive Drug-Resistant Salmonella enterica Isolated From Poultry and Humans: Prevalence and Molecular Determinants Behind the Co-resistance to Ciprofloxacin and Tigecycline. Front. Microbiol. 12:738784. doi: 10.3389/fmicb.2021.738784
Abd El-Ghany WA. 2020. Salmonellosis: A foodborne zoonotic and public health disease in Egypt. J. Infect. Dev. Ctries., 14(7): 674-678. doi: 10.3855/jidc.12739.
Abiodun A, Lloyd W, Lisa M, Bowen L, George J, Alva SJ. 2014. Resistance to antimicrobial agents among Salmonella isolates recovered from layer farms and eggs in the Caribbean region’, Journal of Food Protection, 77(12): 2153–2160. doi: 10.4315/0362-028X.JFP-14-162.
Ahmed AO, Raji MA, Mamman PH, Kwanashie CN, Raufu IA, Aremu A, Akorede GJ. 2019. Salmonellosis: Serotypes, prevalence and multi-drug resis¬tant profiles of Salmonella enterica in selected poultry farms, Kwara State, North Central Nigeria. Onderstepoort J. Vet. Res., 86(1): a1667. doi: 10.4102/ojvr.v86i1.1667
Akond MA, Shirin M, Alam S, Hassan SM, Rahman MM, Hoq M. 2012. Frequency of drug resistant Salmonella spp. isolated from poultry samples in Bangladesh. Stamford J Microbiol., 2(1):15–9. https:// doi.org/10.3329/sjm.v2i1.15207
Al-Mamun MA, Kabir SL, Islam MM, Lubna M, Islam SS, Akhter AT. 2017. Molecular identification and characterization of Salmonella species isolated from poultry value chains of Gazipur and Tangail districts of Bangladesh. Afr J Microbiol Res., 11(11):474–81. https://doi.org/10.5897/ AJMR2017-8431
Andoh LA, Dalsgaard A, Obiri-Danso K, Newman MJ, Barco L, Olsen JE. 2016. Prevalence and antimicrobial resistance of Salmonella serovars isolated from poultry in Ghana. Epidemiol Infect., 144 (15):3288–99. https://doi.org/10.1017/S09502688160011
Asogwa NV, Udeani TK, Obeagu EI, Asogwa BE, Chukwueze CM. 2022. Prevalence of Salmonella species infection in poultry farming systems in Enugu metropolis Nigeria. European journal of pharmaceutical and medical research, 9(4), 87-91 www.ejpmr.com
Barua H, Biswas PK, Olsen KEP, Christensen JP. 2012. Prevalence and Characterization of Motile Salmonella in Commercial Layer Poultry Farms in Bangladesh. PLoS ONE 7(4): e35914. https://doi.org/10.1371/journal.pone.0035914
Barilli E, Bacci C, Villa ZS, Merialdi G, D’Incau M, Brindani F, Vismarra A. 2018. Antimicrobial resistance, biofilm synthesis and virulence genes in Salmonella isolated from pigs bred on intensive farms. Ital. J. Food Saf., 7: 131–137. doi: 10.4081/ijfs.2018.7223
Cantas L, Shah SQ, Cavaco LM, Manaia CM, Walsh F, Popowska M. 2013. A brief multi-disciplinary review on antimicrobial resistance in medicine and its linkage to the global environmental microbiota’, Frontier Microbiology, 4: 96-99. doi: 10.3389/fmicb.2013.00096
Campos J, Mourão J, Peixe L, Antunes P. 2019. Non-typhoidal Salmonella in the pig production chain: A comprehensive analysis of its impact on human health. Pathogens, 8: 19. doi: 10.3390/pathogens8010019.
Clinical and Laboratory Standards Institue (CLSI). 2018. Performance Standards for Antimicrobial Susceptibility Testing 28th Edition. Clinical and Laboratory Standards Institute.
Davies RH, Wales AD. 2010. Investigations into Salmonella contamination in poultry feed-mills in the United Kingdom, Journal of Applied Microbiology, 109: 1430–1440. https://doi.org/10.1111/j.1365-2672.2010.04767.x
Effendi MH, Harijani N, Triningtya NP, Tyasningsih W, Plumeriastuti H. 2019. Prevalence of Pathogenic Escherichia coli Isolated from Sub clinic Mastitis in East Java Province, Indonesia. Indian Vet J 96 (3): 22-25. DOI: 10.13057/biodiv/d220137
Eguale T. 2018. Non-typhoidal Salmonella serovars in poultry farms in central Ethiopia: Prevalence and antimicrobial resistance. BMC Vet Res. 14(1):1–8. https://doi.org/10.1186/s12917-017-1323-x PMID: 29291752
Ejikeugwu C, Afiukwa N, Nwuzo A, Ovia K, Adonu C, Ujam T, Nworie C, Agbai EN, Nwankwo C, Onwuenwunor BO. 2018. Phenotypic detection of metallo-?-lactamase (MBL) and AmpC enzymes among abattoir isolates of Escherichia coli and Klebsiella species in Abakaliki, Nigeria. Trends Med, 18: 1-4. doi: 10.15761/TiM.1000124
European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC) (2022). The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2018/2019. EFSA J., 20, e07209. https://doi.org/10.2903/j.efsa.2022.7209
Fagbamila IO, Barco L, Mancin M. 2017. Salmonella serovars and their distribution in Nigerian commercial chicken layer farms. PLoS One, 12(3): 1-15. doi: 10.1371/journal.pone.0173097.
Faleke OO, Jolayemi KO, Igoh YO, Jibril AH, Ayedun JO. 2017. Salmonella species on meat contact surfaces and processing water in sokoto main market and abattoir, Nigeria. Macedonian Vet. Rev. 40(1): 59–65. https://doi.org/10.1515/macvetrev-2017-0011
Fanissa F, Effendi MH, Tyasningsih W, Ugbo EB. 2022. Multidrug-resistant Salmonella species from chicken meat sold at Surabaya Traditional Markets, Indonesia. Biodiversitas 23: 2823-2829. doi: 10.13057/biodiv/d230606
Govinden U, Mocktar C, Moodley P, Sturm AW, Essack SY. 2008. Characterization of extended-spectrum ?-lactamases in Salmonella spp. at a tertiary hospital in Durban, South Africa’, Diagnostic Microbiology and Infectious Disease, 62(2): 86–91. doi: 10.1016/j.diagmicrobio.2008.04.014
Gymoese P, Sorensen G, Litrup E, Olsen JE, Nielsen EM, Torpdahl M. 2017. Investigation of outbreaks of Salmonella enterica serovar typhimurium and its monophasic variants using whole-genome sequencing, Denmark. Emerg Infect Dis. 23(10):1631–1639. doi: 10.3201/eid2310.161248
Hussein M, Hala K, Khalil A. 2009. Characterization of Salmonella Lipopolysaccharide isolated from poultry farms in Jordan, Dirasat Pure Sciences 36(1): 30–37.
Ibrahim S, Wei Hoong L, Lai Siong Y, Mustapha Z, Zalati CWS, Aklilu E, Mohamad M, Kamaruzzaman NF. 2021. Prevalence of Antimicrobial Resistance (AMR) Salmonella spp. and Escherichia coli Isolated from Broilers in the East Coast of Peninsular Malaysia. Antibiotics, 10, 579. https://doi.org/10.3390/antibiotics10050579
Idowu OF, Lisa B, Marzia M, Jacob K, Sati SN, Paola Z. 2017. Salmonella serovars and their distribution in Nigerian commercial chicken layer farms, PLoS One, 12(3): 41-45. doi: 10.1371/journal.pone.0173097
Jibril AH, Okeke IN, Dalsgaard A, Kudirkiene E, Akinlabi OC. 2020. Prevalence and risk factors of Salmonella in commercial poultry farms in Nigeria. PLOS ONE 15(9): e0238190. https://doi.org/10.1371/journal.pone.0238190
Jun K, Kiyomasa I, Katsuya T, Aiko I, Miwa K, Tamaki S. 2006. 'Characterization of Salmonella isolated in Okinawa, Japan'. Japan Journal of Infectious Disease 59, 15-19. PMID: 16495628.
Kong-Ngoen T, Santajit S, Tunyong W, Pumirat P, Sookrung N, Chaicumpa W, Indrawattana N. 2022. Antimicrobial Resistance and Virulence of Non-Typhoidal Salmonella from Retail Foods Marketed in Bangkok, Thailand. Foods, 11: 661. https://doi.org/10.3390/foods11050661
Lai J, Wu C, Wu C, Qi J, Wang Y, Wang H, Liu Y, Shen J. 2014. Serotype distribution and antibiotic resistance of Salmonella in food-producing animals in Shandong province of China, 2009 and 2012. Int. J. Food Microbiol., 180, 30–38. doi: 10.1016/j.ijfoodmicro.2014.03.030.
Lettini AA, Vo Than T, Marafin E, Longo A, Antonello K, Zavagnin P. 2016. Distribution of Salmonella Serovars and Antimicrobial Susceptibility from Poultry and Swine Farms in Central Vietnam. Zoonoses Public Health, 63(7):569-576. doi: 10.1111/zph.12265
Mahmud MS, Bari ML, Hossain MA. 2011. Prevalence of Salmonella serovars and antimicrobial resistancemprofiles in poultry of Savar area, Bangladesh. Foodborne Pathog Dis., 8(10):1111–8. https://doi.org/10.1089/fpd.2011.0917 PMID: 21689000
Medalla F, Gu W, Mahon BE, Judd M, Folster J, Griffin PM. 2017. Estimated Incidence of Antimicrobial Drug – Resistant Nontyphoidal Salmonella Infections, United States, 2004-2012. Emerg Infect Dis., 23(1):4–12. doi: 10.3201/eid2301.160771
Mridha D, Uddin MN, Alam B, Akhter AT, Islam SS, Islam MS. 2020. Identification and characterization of Salmonella spp. from samples of broiler farms in selected districts of Bangladesh. Vet World. 13(2):275. https://doi.org/10.14202/vetworld.2020.275-283 PMID: 32255969
Musawa AI, Bashiru G, Al-Rasheed A, Yakubu Y, Jibril AH, Ballah FM, Sidi S, Lawal N, Bala JA, Odhah MN, Muhammad N, Umar M. 2021. Prevalence and antimicrobial susceptibility profiling of salmonella isolated from poultry products sold in sokoto metropolis, nigeria. J. Anim. Health Prod. 9(2): 148-155. doi http://dx.doi.org/10.17582/journal.jahp/2021/9.2.148.155
National Bureau of Statistics, 2012. Federal Republic of Nigeria, Annual Abstract of Statistics, 2012. www.nigerianstat.gov.ng
Nguyen TK, Nguyen LT, Chau TTH, Nguyen TT, Tran BN, Taniguchi T, Hayashidani H, Ly KTL. 2021. Prevalence and antibiotic resistance of Salmonella isolated from poultry and its environment in the Mekong Delta, Vietnam, Veterinary World, 14(12): 3216-3223. doi: www.doi.org/10.14202/vetworld.2021.3216-3223
Odoch T, Wasteson Y, L’Abe´e-Lund T, Muwonge A, Kankya C, Nyakarahuka L. 2017. Prevalence, antimicrobial susceptibility and risk factors associated with non-typhoidal Salmonella on Ugandan layer hen farms. BMC Vet Res., 13(1):1–10. https://doi.org/10.1186/s12917-016-0931-1 PMID: 28049469
Permatasari DA, Witaningrum AM, Wibisono FJ, Effendi MH. 2020. Detection and prevalence of Multidrug Resistant Klebsiella pneumoniae strains isolated from poultry farms in Blitar, Indonesia. Biodiversitas 21:4642-4647. https://doi.org/10.13057/biodiv/d211024
P?awinska-Czarnak J, Wódz K, Kizerwetter-Swida M, Bogdan J, Kwieci ´nski P, Nowak T, Strza?kowska Z, Anusz K. 2022. Multi-Drug Resistance to Salmonella spp. When Isolated from Raw Meat Products. Antibiotics, 11, 876. https://doi.org/10.3390/ antibiotics11070876.
Putra AR, Effendi MH, Koesdarto S, Suwarno S, Tyasningsih W, Estoepangestie AT. 2020. Detection of the extended spectrum ?-lactamase produced by Escherichia coli from dairy cows by using the vitek-2 method in Tulungagung Regency, Indonesia. Iraqi Journal of Veterinary Sciences, 34(1), 203-207. https://doi.org/10.33899/ijvs.2019.125707.1134
Riwu KHP, Effendi MH, Rantam FA. 2020. A review of extended-spectrum ?-Lactamase (ESBL) producing Klebsiella pneumoniae and Multidrug-Resistant (MDR) on companion animals. Syst Rev Pharm 11 (7): 270-277. DOI: 10.31838/srp.2020.7.43.
Robertson J, Yoshida C, Kruczkiewicz P, Nadon C, Nichani A, Taboada EN. 2018. Comprehensive assessment of the quality of Salmonella whole genome sequence data available in public sequence databases using the Salmonella in silico Typing Resource (SISTR). Microb genomics 4(2):14-18. doi: 10.1099/mgen.0.000151
Rodriguez-Rivera LD, Wright EM, Siler JD, Elton M, Cummings KJ, Warnick LD, Wiedmann M. 2014. Subtype analysis of Salmonella isolated from sub-clinically infected dairy cattle and dairy farm environments reveals the presence of both human-and bovine-associated subtypes. Vet Microbiol., 170 (4): 307–316. doi: 10.1016/j.vetmic.2014.02.013
Sarker BR, Ghosh S, Chowdhury S, Dutta A, Chandra Deb L, Sarker BK. 2021. Prevalence and antimicrobial susceptibility profiles of non-typhoidal Salmonella isolated from chickens in Rajshahi, Bangladesh. Vet Med Sci., 7(3):820–830. https://doi.org/10.1002/vms3.440 PMID: 33527778
Slader J, Domingue G, Jorgensen F, McAlpine K, Owen RJ, Bolton FJ, Humphrey TJ. 2002. Impact of transport crate reuse and of catching and processing on Campylobacter and Salmonella contamination of broiler chickens. Appl. Environ. Microbiol., 68:713–719. doi: 10.1128/AEM.68.2.713-719.2002.
Siddiky NA, Sarker S, Khan SR, Rahman T, Kafi A, Samad MA. 2022. Virulence and antimicrobial resistance profile of non-typhoidal Salmonella enterica serovars recovered from poultry processing environments at wet markets in Dhaka, Bangladesh. PLoS ONE 17(2): e0254465. https://doi.org/10.1371/journal.pone.0254465.
Sohail MN, Rathnamma D, Chandra PS, Isloor S, Naryanaswamy HD, Wilfred RS, Veeregowda BM. 2021. Salmonella from Farm to Table: Isolation, Characterization, and Antimicrobial Resistance of Salmonella from Commercial Broiler Supply Chain and Its Environment. BioMed Research International, Volume 2021, Article ID 3987111, 12 pages https://doi.org/10.1155/2021/3987111
Sin M, Yoon S, Kim YB, Noh EB, Seo KW, Lee YJ. 2020. Molecular characteristics of antimicrobial resistance determinants and integrons in Salmonella isolated from chicken meat in Korea. J Appl Poult Res 29 (2): 502-514. doi: 10.1016/j.japr.2019.12.010.
Useh NM, Ngbede EO, Akange N, Thomas M, Foley A, Keena MC, Nelson E, Christopher-Hennings J, Tomita M, Suzuki H, Scaria J. 2016. Draft genome sequences of 37 Salmonella enterica strains isolated from poultry sources in Nigeria. Genome Announc 4(3):e00315-16. doi:10.1128/genomeA.00315-16.
Tack B, Vanaenrode J, Jan YV, Jaan T, Jan J. 2020. Invasive non-typhoidal Salmonella infections in sub-Saharan Africa: a systematic review on antimicrobial resistance and treatment. BMC Medicine, 18:212. https://doi.org/10.1186/s12916-020-01652-4
Telli AE, Biçer Y, Telli N, Güngör C, Turkal G, Onmaz NE. 2022. Pathogenic Escherichia coli and Salmonella spp. in chicken rinse carcasses: Isolation and genotyping by ERIC-PCR. Pak Vet J, 42(4): 493- 498. http://dx.doi.org/10.29261/pakvetj/2022.049
Thliza LA, Khan AU, Dangora DB, Yahaya A. 2015. Study of some bacterial load of some brands of sachet water sold in Ahmadu Bello University (Main Campus), Zaria, Nigeria. International Journal of current Science, 14:91-97. Corpus ID: 110256201.
Wibisono FJ, Sumiarto B, Untari T, Effendi MH, Permatasari DA, Witaningrum AM. 2020a. Short Communication: Pattern of antibiotic resistance on extended-spectrum beta-lactamases genes producing Escherichia coli on laying hens in Blitar, Indonesia. Biodiversitas 21: 4631-4635. https://doi.org/10.13057/biodiv/d211022
Wibisono FM, Wibisono FJ, Effendi MH, Plumeriastuti H, Hidayatullah AR, Hartadi EB, Sofiana ED. 2020b. A Review of Salmonellosis on poultry farms: Public Health Importance. Syst Rev Pharm 11 (9): 481-486. DOI: 10.31838/srp.2020.9.69.
Wibisono FM, Faridah HD, Wibisono FJ, Tyasningsih W, Effendi MH, Witaningrum AM, Ugbo EN. 2021. Detection of invA virulence gene of multidrug-resistant Salmonella species isolated from the cloacal swab of broiler chickens in Blitar district, East Java, Indonesia, Veterinary World, 14(12): 3126-3131. doi: www.doi.org/10.14202/vetworld.2021.3126-3131
Wibisono FJ, Rahmaniar RP, Syaputra DE, Zuriya Z, Aziz KM, Ikeng LD, Effendi MH, Bernard AN. 2023. Risk Factors for Non-typhoidal Salmonella Contamination in chicken meat: A cross-sectional study on Traditional Markets in Surabaya. Adv. Life Sci. 10(2): 282-288.
Yanestria SM, Rahmaniar RP, Wibisono FJ, Effendi MH. 2019. Detection of invA gene of Salmonella from milkfish (Chanos chanos) at Sidoarjo wet fish market, Indonesia, using polymerase chain reaction technique. Veterinary World. 12(1): 170-175
Yang X, Wu Q, Zhang J, Huang J, Chen L, Wu S, Zheng H, Wang J, Chen M, Wu H, Gu Q, Wei X. 2019. Prevalence, bacterial load, and antimicrobial resistance of Salmonella serovars isolated from retail meat and meat products in China. Front Microbiol 10: 2121. doi: 10.3389/fmicb.2019.02121

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